Diet composition of an escaped captive‐born southern tamandua (Tamandua tetradactyla) in a nonnative habitat in Asia

Abstract Studies on the role of natural predatory instincts in captive‐born mammalian myrmecophagy are rare. Consequently, researchers rely extensively on case reports to learn more about the contexts in which predatory behavior occurs among such animals. In this study, we recorded an uncommon case of a captive‐born southern tamandua (Tamandua tetradactyla) that accidentally escaped from a zoo into a nonnative habitat in Asia. The southern tamandua was found alive 3 months later. Two fresh fecal samples were obtained, and the diet composition was examined. Three termite species (one family, three genera), and 14 ant species (four subfamilies, nine genera) were identified in the fecal samples. The studied southern tamandua preyed on terrestrial and arboreal ants and termites, as the wild populations of its species do. Ants of the subfamily Myrmicinae and termites of the subfamily Nasutitermitinae were the most abundant prey items in the samples, which is consistent with related reports on the wild populations. Soldier ants constituted <1% of the prey items in the fecal samples, suggesting that the southern tamandua likely avoided preying on ants of the soldier caste. Fungus‐growing termites Odontotermes (Isoptera: Macrotermitinae), which are not native to neotropical regions, were also ingested by the southern tamandua. This study provides information on how a captive‐born mammalian myrmecophagy applies its natural feeding instincts in nonnative natural settings.

Consequently, meeting the dietary and behavioral needs of captive and captive-born tamanduas, such as those bred in modern zoos, is challenging (Oyarzun et al., 1996). Captive individuals typically receive artificial or commercial feed (Catapani et al., 2018).
The abundance and ready availability of food supplies in captivity may affect animals' natural predatory instincts (Maple, 1980;Poole, 1987). The factors that affect the survival of captive-born or reintroduced animals in the wild include prerelease training, habitat characteristics, food supplies, and anthropogenic disturbances in the environment (Maran et al., 2009). Jiménez Pérez et al. (2015) reported the survival rate of reintroduced giant anteaters in Iberá Nature Reserve, Argentina was 76% (11 died out of 47 released animals). There have been few studies on the role of natural predatory instincts in captive-born mammalian myrmecophagy in the wild. Here, we report a rare case of a 3-year-old captive-born female southern tamandua that accidentally escaped from Taipei Zoo into a nonnative habitat. The southern tamandua had not previously lived in the wild nor fed on natural prey items. The studied southern tamandua was found alive after 3 months in the wild. After locating the southern tamandua, we collected two fresh fecal samples and investigated the southern tamandua's diet composition. Specialist species are more susceptible to nonnatives diet than are generalist species because of their narrow feeding habits. Therefore, how this captive-born southern tamandua applied its natural feeding instincts in the wild and how it selected nonnative prey are of interest. We conducted this study to analyze what prey items the captive-born southern tamandua consumed in the nonnative habitat and whether these prey items were similar to those consumed by tamanduas in native habitats. Given that this is the first report of a captive-born southern tamandua surviving for 3 months in a nonnative habitat, it provides valuable insights regarding the adaptation of exotic species and the detailed dietary composition of the southern tamandua, further elucidating the characteristics and behaviors of this highly specialized predator.

| Study area
The study area is close to Taipei Zoo (24.994676, 121.586293) in northern Taiwan (Figure 1b). Taipei Zoo is bordered by hills to the south and east and has an average elevation of 100 m. The climate of northern Taiwan is generally subtropical. The average monthly temperature in 2020 was 22.6°C (range: 16.2°C in January to 28.3°C in July; ShengKeng station, Taiwan Central Weather Bureau, http:// www.cwb.gov.tw). The annual precipitation in 2020 was 2132.5 mm (Taiwan Central Weather Bureau). The vegetation cover of the study area consists of evergreen broad-leaved forests, bamboo forests, grasslands, and farmlands.

| Subject
The southern tamandua was captive-born and brought to Taipei Zoo at 12 months in August 2018. The captive environment at the zoo had natural structural features, including tree trunks, branches, and plants with dirt substrates. The southern tamandua received 300 g of feed, composed of meal worms, bee pupae, fruits, chitin powder, and vegetables, daily. As of November 3, 2019, the southern tamandua weighed 6.2 kg. On November 28, 2019, the southern tamandua was paired. On May 10, 2020, the southern tamandua gave birth. The cub was nursed by the studied southern tamandua. At 2:30 a.m. on September 1, 2020, the studied southern tamandua escaped from Taipei Zoo with the cub and reached a nearby forest (Figure 1b). The cub was found alive the next day in the culvert of the zoo. After 97 days, on December 6, 2020, the studied southern tamandua was found in a tree den in a secondary forest 3 km away from the zoo (Figure 1b), and its identity was confirmed through microchip scanning. The southern tamandua was subsequently brought to Taipei Zoo for clinical examination. Its body weight was 5.5 kg at the time.
On the same day, the southern tamandua received 450 g of regular feed.

| Analysis of fecal composition
On December 7, two of the southern tamandua's fecal samples were collected from its enclosure. The feces from which the samples were collected were defecated 30 min apart. In captivity, tamanduas normally defecate every 2 to 6 days (Meritt, 1975), indicating the southern tamandua feces collected in this study presumably represented its diet composition in the wild from within the preceding week. Both of the fecal samples consisted of the cuticular remains of ants and termites. We sampled 1 g of dry mass from each defecation for prey composition analysis. We performed fecal content analysis and prey item identification to extract prey items and debris by following the fecal filtering procedures proposed by Sun et al. (2019).
The filtered prey items were macrophotographed and digitized (see Sun et al., 2019 for details). The termites and ants were identified to species level, and the number of individuals was counted using the macrophotographs (Sun et al., 2019). The morphological characteristics of ant head capsules were used for species identification and individual quantification. In termites, the left mandible is more morphologically diverse than the right mandible, and the numbers of left and right mandibles in the feces of animals consuming termites do not differ significantly (Liang, 2017). We therefore used termite left mandibles for species identification and individual quantification.
For conehead soldier termites of genus Nasutitermes, head capsules were used for species identification and individual quantification (as illustrated in Figure 2). Finally, the prey item information collected in this study (such as subfamily, genus, and lifestyle) was compared with that reported in previously published literature.

| RE SULTS
A total of 1019 termite individuals across three species (one family, three genera) and 583 ant individuals across 14 species (four subfamilies, nine genera) were identified from the fecal samples (Table 1)

| DISCUSS ION
Although the findings of this study are based on limited fecal samples, we were able to collect detailed information regarding the prey composition of the southern tamandua. Our findings also provide insights into the feeding adaptation of a captive-born southern tamandua in a nonnative habitat. Overall, the prey composition of the studied southern tamandua exhibited some common patterns with those of wild populations of tamanduas in South America. For example, the studied southern tamandua consumed both terrestrial and arboreal ants and termites, which is consistent with previous records (Table 1).
The ant subfamilies Myrmicinae and Formicinae exhibit the highest species richness in the diets of wild tamanduas (Table 1). However, in this study, high species richness was only observed for the subfamily Myrmicinae. This was likely due to the limited number of fecal samples collected or the availability of Myrmicinae is generally abundant in suburban Taiwan. In addition, soldier ants comprised <1% of the ant individuals present in the fecal samples, which suggests that the southern tamandua likely avoided preying on colonies with large numbers of ants of the soldier caste. Social insects typically have well-developed chemical and physical defenses (Redford, 1985), and the defense behavior of ants and termites is effective in repelling anteaters .
Montomery (Montgomery, 1985) and Lubin and Montgomery (1981) reported that Nasutitermes termites are an important part of the diets of both tamandua species. Nasutitermes parvonasutus are commonly found in suburban Taiwan (Liang & Li, 2016) and were the species of which the southern tamandua in this study consumed the most. Although N. parvonasutus do not inhabit neotropical regions, Nasutitermes spp. are found commonly in south America (Constantino, 2020). We speculated the studied southern tamandua preyed on a significant amount of N. parvonasutus likely due to the display of their natural predatory instincts. N. parvonasutus does not build arboreal nests but build shelter tubes on tree trunks; mature colonies of this species may also build nests underground (Liang & Li, 2016). In addition, Nasutitermes soldiers are present in greater numbers in nests and in lower numbers in shelter tubes and decomposing wood; and the defense of soldiers is effective in repelling large vertebrate predators, such as tamanduas (Lubin & Montgomery, 1981). Remarkably, a termitophilous beetle,  (Gallo et al., 2017;Reiss, 2000). In addition, only major worker of O. formosanus was present in the fecal samples; no minor workers, alates, or nymphs were present. Generally, major worker termites are responsible for foraging and building shelter tubes on the ground, whereas minor workers are more commonly involved in feeding and nursing within underground nest chambers (de Oliveira et al., 2021;Wang et al., 2009). Hence, we speculated that the southern tamandua fed on O. formosanus foraging aboveground instead of excavating underground nest chambers.
Reticulitermes are also not native to South America, and they were recently introduced to Chile, Argentina, and Uruguay (Austin et al., 2005;Constantino, 2002). The distribution of the introduced Reticulitermes does not overlap with that of south tamandua. R. flaviceps is an endemic species and only found in Taiwan, and they are commonly found in lowland forest and also build foraging tubes on the ground (Wu et al., 2019). Hence, we believe the studied tamandua preyed on R. flaviceps likely due to the availability on the ground.

F I G U R E 2
Macrophotograph of cuticular remains of prey in southern tamandua (Tamandua tetradactyla) feces. The feces were collected from a captive-born southern tamandua that escaped from Taipei zoo and lived in the wild for 3 months in Taiwan. Scale bar = 2 mm. TA B L E 1 Review of Tamandua spp. diet composition compared with that of the southern tamandua from the present study. The first two columns of number of prey species consumed are from previous studies.  (Yen et al., 2019).
In summary, this study reveals the adaptations of a captive-born animal in a nonnative habitat and provides insights into how captiveborn animals apply their natural feeding instincts in natural settings.
To expand upon the current results and further elucidate the dietary characteristics of tamanduas in natural and captive settings, the gut microbiomes of wild and captive southern tamandua were analyzed; the results will be provided in a future article.

ACK N OWLED G M ENTS
The authors thank Tsung-Yi Liu and Shao Weng, staff members of

CO N FLI C T O F I NTE R E S T
None declared.

DATA AVA I L A B I L I T Y S TAT E M E N T
All the data are presented in the article (Table 1) Foraging phenology of the fungus-growing termite Odontotermes